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Role of murine intestinal interleukin-1 receptor 1-expressing lymphoid tissue inducer-like cells in Salmonella infection.

Chen VL, Surana NK, Duan J, Kasper DL - PLoS ONE (2013)

Bottom Line: These cells are significant producers of IL-22, and this IL-22 production depends on IL-1R1 signaling.LTi-like cells are required for defense against Salmonella enterica serovar Typhimurium.Moreover, colonic LTi-like cell numbers depend on the presence of the intestinal microbiota.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology and Immunobiology, Harvard Medical School, Boston, Massachusetts, USA.

ABSTRACT
Interleukin (IL)-1 signaling plays a critical role in intestinal immunology. Here, we report that the major population of intestinal lamina propria lymphocytes expressing IL-1 receptor 1 (IL-1R1) is the lymphoid tissue inducer (LTi)-like cell, a type of innate lymphoid cell. These cells are significant producers of IL-22, and this IL-22 production depends on IL-1R1 signaling. LTi-like cells are required for defense against Salmonella enterica serovar Typhimurium. Moreover, colonic LTi-like cell numbers depend on the presence of the intestinal microbiota. LTi-like cells require IL-1R1 for production of protective cytokines and confer protection in infectious colitis, and their cell numbers in the colon depend upon having a microbiome.

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Colonic LTi-like cells are significant innate producers of IL-22.(A) Representative FACS histogram depicting percentage of CD4+ LTi-like cells that produce IL-22 under control conditions (left panel) and in DSS colitis (right panel) in Rag1−/− C57BL/6J mice. (B) Graph summarizing percentage of CD4+ LTi-like cells producing IL-22. (C) Representative scatter plot depicting the phenotype of IL-22-producing lymphocytes under control conditions (left panel) and in DSS colitis (right panel) in Rag1−/− C57BL/6J mice. Gated on IL-22+ lymphocytes. (D) Graph depicting percentage of IL-22-producing lymphocytes that are CD4+ LTi-like cells. All graphs represent three independent experiments. *, p<0.05; NS, not significant. For box and whisker plots, line represents median, box represents 25th to 75th percentile range, and whiskers represent range.
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pone-0065405-g002: Colonic LTi-like cells are significant innate producers of IL-22.(A) Representative FACS histogram depicting percentage of CD4+ LTi-like cells that produce IL-22 under control conditions (left panel) and in DSS colitis (right panel) in Rag1−/− C57BL/6J mice. (B) Graph summarizing percentage of CD4+ LTi-like cells producing IL-22. (C) Representative scatter plot depicting the phenotype of IL-22-producing lymphocytes under control conditions (left panel) and in DSS colitis (right panel) in Rag1−/− C57BL/6J mice. Gated on IL-22+ lymphocytes. (D) Graph depicting percentage of IL-22-producing lymphocytes that are CD4+ LTi-like cells. All graphs represent three independent experiments. *, p<0.05; NS, not significant. For box and whisker plots, line represents median, box represents 25th to 75th percentile range, and whiskers represent range.

Mentions: Given previous work demonstrating that LTi cells are a major source of IL-22 in the small intestine [26], we sought to determine whether colonic LTi-like cells are also a major producer of IL-22 under both healthy and inflammatory conditions. We induced colitis using the well-characterized DSS model, which is a chemical colitis mediated primarily by innate immune cells [30]. Rag1−/− mice were used because the adaptive immune system suppresses the function of LTi-like cells [26] and we were interested primarily in the contribution of LTi-like cells to innate immunity. DSS colitis in Rag1−/− mice induces colonic LTi-like cells to produce IL-22: the percentage of LTi-like cells producing IL-22 increases from ∼13% in healthy (control) conditions to ∼37% in inflammatory (DSS) conditions (Fig. 2A and 2B). In addition, colonic LTi-like cells constitute a substantial proportion of the IL-22-producing cells in the cLP of Rag1−/− mice (Fig. 2C and 2D), both in health and in the setting of colitis. Overall, these data demonstrate that cLP CD4+ LTi-like cells are important innate producers of IL-22 and upregulate IL-22 production in the setting of intestinal inflammation.


Role of murine intestinal interleukin-1 receptor 1-expressing lymphoid tissue inducer-like cells in Salmonella infection.

Chen VL, Surana NK, Duan J, Kasper DL - PLoS ONE (2013)

Colonic LTi-like cells are significant innate producers of IL-22.(A) Representative FACS histogram depicting percentage of CD4+ LTi-like cells that produce IL-22 under control conditions (left panel) and in DSS colitis (right panel) in Rag1−/− C57BL/6J mice. (B) Graph summarizing percentage of CD4+ LTi-like cells producing IL-22. (C) Representative scatter plot depicting the phenotype of IL-22-producing lymphocytes under control conditions (left panel) and in DSS colitis (right panel) in Rag1−/− C57BL/6J mice. Gated on IL-22+ lymphocytes. (D) Graph depicting percentage of IL-22-producing lymphocytes that are CD4+ LTi-like cells. All graphs represent three independent experiments. *, p<0.05; NS, not significant. For box and whisker plots, line represents median, box represents 25th to 75th percentile range, and whiskers represent range.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3672157&req=5

pone-0065405-g002: Colonic LTi-like cells are significant innate producers of IL-22.(A) Representative FACS histogram depicting percentage of CD4+ LTi-like cells that produce IL-22 under control conditions (left panel) and in DSS colitis (right panel) in Rag1−/− C57BL/6J mice. (B) Graph summarizing percentage of CD4+ LTi-like cells producing IL-22. (C) Representative scatter plot depicting the phenotype of IL-22-producing lymphocytes under control conditions (left panel) and in DSS colitis (right panel) in Rag1−/− C57BL/6J mice. Gated on IL-22+ lymphocytes. (D) Graph depicting percentage of IL-22-producing lymphocytes that are CD4+ LTi-like cells. All graphs represent three independent experiments. *, p<0.05; NS, not significant. For box and whisker plots, line represents median, box represents 25th to 75th percentile range, and whiskers represent range.
Mentions: Given previous work demonstrating that LTi cells are a major source of IL-22 in the small intestine [26], we sought to determine whether colonic LTi-like cells are also a major producer of IL-22 under both healthy and inflammatory conditions. We induced colitis using the well-characterized DSS model, which is a chemical colitis mediated primarily by innate immune cells [30]. Rag1−/− mice were used because the adaptive immune system suppresses the function of LTi-like cells [26] and we were interested primarily in the contribution of LTi-like cells to innate immunity. DSS colitis in Rag1−/− mice induces colonic LTi-like cells to produce IL-22: the percentage of LTi-like cells producing IL-22 increases from ∼13% in healthy (control) conditions to ∼37% in inflammatory (DSS) conditions (Fig. 2A and 2B). In addition, colonic LTi-like cells constitute a substantial proportion of the IL-22-producing cells in the cLP of Rag1−/− mice (Fig. 2C and 2D), both in health and in the setting of colitis. Overall, these data demonstrate that cLP CD4+ LTi-like cells are important innate producers of IL-22 and upregulate IL-22 production in the setting of intestinal inflammation.

Bottom Line: These cells are significant producers of IL-22, and this IL-22 production depends on IL-1R1 signaling.LTi-like cells are required for defense against Salmonella enterica serovar Typhimurium.Moreover, colonic LTi-like cell numbers depend on the presence of the intestinal microbiota.

View Article: PubMed Central - PubMed

Affiliation: Department of Microbiology and Immunobiology, Harvard Medical School, Boston, Massachusetts, USA.

ABSTRACT
Interleukin (IL)-1 signaling plays a critical role in intestinal immunology. Here, we report that the major population of intestinal lamina propria lymphocytes expressing IL-1 receptor 1 (IL-1R1) is the lymphoid tissue inducer (LTi)-like cell, a type of innate lymphoid cell. These cells are significant producers of IL-22, and this IL-22 production depends on IL-1R1 signaling. LTi-like cells are required for defense against Salmonella enterica serovar Typhimurium. Moreover, colonic LTi-like cell numbers depend on the presence of the intestinal microbiota. LTi-like cells require IL-1R1 for production of protective cytokines and confer protection in infectious colitis, and their cell numbers in the colon depend upon having a microbiome.

Show MeSH
Related in: MedlinePlus